scholarly journals External α-carbonic anhydrase and solute carrier 4 are required for bicarbonate uptake in a freshwater angiosperm

2020 ◽  
Vol 71 (19) ◽  
pp. 6004-6014
Author(s):  
Wenmin Huang ◽  
Shijuan Han ◽  
Hongsheng Jiang ◽  
Shuping Gu ◽  
Wei Li ◽  
...  

Abstract The freshwater monocot Ottelia alismoides is the only known species to operate three CO2-concentrating mechanisms (CCMs): constitutive bicarbonate (HCO3–) use, C4 photosynthesis, and facultative Crassulacean acid metabolism, but the mechanism of HCO3– use is unknown. We found that the inhibitor of an anion exchange protein, 4,4'-diisothio-cyanatostilbene-2,2'-disulfonate (DIDS), prevented HCO3– use but also had a small effect on CO2 uptake. An inhibitor of external carbonic anhydrase (CA), acetazolamide (AZ), reduced the affinity for CO2 uptake but also prevented HCO3– use via an effect on the anion exchange protein. Analysis of mRNA transcripts identified a homologue of solute carrier 4 (SLC4) responsible for HCO3– transport, likely to be the target of DIDS, and a periplasmic α-carbonic anhydrase 1 (α-CA1). A model to quantify the contribution of the three different pathways involved in inorganic carbon uptake showed that passive CO2 diffusion dominates inorganic carbon uptake at high CO2 concentrations. However, as CO2 concentrations fall, two other pathways become predominant: conversion of HCO3– to CO2 at the plasmalemma by α-CA1 and transport of HCO3– across the plasmalemma by SLC4. These mechanisms allow access to a much larger proportion of the inorganic carbon pool and continued photosynthesis during periods of strong carbon depletion in productive ecosystems.

1998 ◽  
Vol 76 (6) ◽  
pp. 1043-1051 ◽  
Author(s):  
Ilana Berman-Frank ◽  
Jonathan Erez ◽  
Aaron Kaplan

The physiological, biochemical, and genetic aspects of inorganic (Ci) carbon uptake in aquatic plants and algae have been studied extensively. Yet, to date, few studies examined these questions on dominant phytoplankton populations in their natural environment. Lake Kinneret, Israel, provides a good example of a system in which changes in CO2 availability play a vital role in the ecophysiology of inorganic carbon uptake and in the population dynamics during the annual bloom of the dinoflagellate Peridinium gatunense Nygaard. In this study we investigated whether the availability of CO2(aq) limited growth rates and primary productivity of in situ populations of P. gatunense and focused on the role of adaptive mechanisms for Ci uptake. At the onset of the bloom, when epilimnetic pH was low ( = 8) and Ci concentrations were high ( = 2.5 mM), carbonic anhydrase activity and cellular affinity to CO2(aq) were comparatively low. At this time photosynthetic rates, quantum yields, and in situ growth rates were high. As P. gatunense biomass increased, inorganic carbon decreased by 40%, while CO2(aq) concentrations declined 50-fold to values less than 2 µM. The algae adapted by acquiring a CO2-concentrating mechanism indicated by (i) intracellular Ci-concentrations higher by a factor of 5-70 relative to the ambient Ci; (ii) levels of carbonic anhydrase activity higher by 5- to 50-fold than those at the beginning of the bloom; and (iii) enhanced affinity for Ci and CO2(aq) 3- and 40-fold higher, respectively, than affinities at the start of the bloom. These mechanistic changes in carbon uptake were reflected in declining photosynthetic rates and quantum yields as well as in the carbon isotopic composition with lower fractionation (13C enrichment) of the algae as the bloom progressed. Finally, despite induction of adaptive uptake mechanisms to low CO2 availability; scarcity of other nutrients combined with low CO2 concentrations, increased temperatures, and increased turbulence cause a decline in in situ growth rates and the collapse of the dinoflagellate biomass.Key words: dinoflagellates, inorganic carbon uptake, CCM, carbonic anhydrase, Peridinium gatunense.


1998 ◽  
Vol 76 (6) ◽  
pp. 1025-1034 ◽  
Author(s):  
James V Moroney ◽  
Zhi-Yuan Chen

The role of the chloroplast in the adaptation to low CO2 by eukaryotic algae is reviewed. Eukaryotic algae can grow on very low CO2 levels because of the presence of a CO2 concentrating mechanism (CCM). This review is focused on the localization of key photosynthetic enzymes such as ribulose-1,5-bisphosphate carboxylase-oxygenase (Rubisco) and carbonic anhydrase as well as the location of presumptive components of the CCM and photorespiratory cycle within the chloroplast. Previous immunolocalization studies place as much as 99% or as little as 5% of the cell's Rubisco in the chloroplast pyrenoid. These different results are summarized, and an alternative explanation is provided. The different results appear to be due to the growth regime of the algae as well as differences in quantitation. Evidence suggests that a large majority of Rubisco is located within the pyrenoid. We have also summarized the recent discovery of a thylakoid-bound carbonic anhydrase that is essential to growth on low CO2. A model depicting a possible role for this carbonic anhydrase in photosynthesis is presented.Key words: chloroplast, algae, pyrenoid, carbonic anhydrase, photosynthesis.


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